scholarly journals Evidence of multifaceted functions of codon usage in translation within the model beetle Tribolium castaneum

2019 ◽  
Author(s):  
Carrie A. Whittle ◽  
Arpita Kulkarni ◽  
Cassandra G. Extavour
Keyword(s):  
Codon Usage ◽  
Tribolium Castaneum ◽  
Germ Line ◽  
Synonymous Codon ◽  
Trna Genes ◽  
Optimal Codons ◽  
Gene Copies ◽  
Highly Expressed Genes ◽  
Codon Use ◽  
Multicellular Organisms

AbstractSynonymous codon use is non-random. Codons most used in highly transcribed genes, often called optimal codons, typically have high gene counts of matching tRNA genes (tRNA abundance) and promote accurate and/or efficient translation. Non-optimal codons, those least used in highly expressed genes, may also affect translation. In multicellular organisms, codon optimality may vary among tissues. At present however, codon use remains poorly understood in multicellular organisms. Here, we studied codon usage of genes highly transcribed in germ line (testis, ovary) and somatic tissues (gonadectomized males and females) of the beetle Tribolium castaneum. The results demonstrate that: 1) the majority of optimal codons were organism-wide, the same in all tissues, and had numerous matching tRNA gene copies (Opt-codon↑tRNAs), consistent with translational selection; 2) some optimal codons varied among tissues, suggesting tissue-specific tRNA populations; 3) wobble tRNA were required for translation of certain optimal codons (Opt-codonwobble), possibly allowing precise translation and/or protein folding; and 4) remarkably, some non-optimal codons had abundant tRNA genes (Nonopt-codon↑tRNAs), and genes using those codons were tightly linked to ribosomal and stress-response functions. Thus, Nonopt-codon↑tRNAs codons may regulate translation of specific genes. Together, the evidence suggests that codon use and tRNA genes regulate multiple translational processes in T. castaneum.

scholarly journals Evidence of multifaceted functions of codon usage in translation within the model beetle Tribolium castaneum

DNA Research ◽  
2019 ◽  
Vol 26 (6) ◽  
pp. 473-484
Author(s):  
Carrie A Whittle ◽  
Arpita Kulkarni ◽  
Cassandra G Extavour
Keyword(s):  
Codon Usage ◽  
Tribolium Castaneum ◽  
Germ Line ◽  
Synonymous Codon ◽  
Trna Genes ◽  
Optimal Codons ◽  
Gene Copies ◽  
Highly Expressed Genes ◽  
High Gene ◽  
Codon Use

Abstract Synonymous codon use is non-random. Codons most used in highly transcribed genes, often called optimal codons, typically have high gene counts of matching tRNA genes (tRNA abundance) and promote accurate and/or efficient translation. Non-optimal codons, those least used in highly expressed genes, may also affect translation. In multicellular organisms, codon optimality may vary among tissues. At present, however, tissue specificity of codon use remains poorly understood. Here, we studied codon usage of genes highly transcribed in germ line (testis and ovary) and somatic tissues (gonadectomized males and females) of the beetle Tribolium castaneum. The results demonstrate that: (i) the majority of optimal codons were organism-wide, the same in all tissues, and had numerous matching tRNA gene copies (Opt-codon↑tRNAs), consistent with translational selection; (ii) some optimal codons varied among tissues, suggesting tissue-specific tRNA populations; (iii) wobble tRNA were required for translation of certain optimal codons (Opt-codonwobble), possibly allowing precise translation and/or protein folding; and (iv) remarkably, some non-optimal codons had abundant tRNA genes (Nonopt-codon↑tRNAs), and genes using those codons were tightly linked to ribosomal and stress-response functions. Thus, Nonopt-codon↑tRNAs codons may regulate translation of specific genes. Together, the evidence suggests that codon use and tRNA genes regulate multiple translational processes in T. castaneum.

scholarly journals Adaptation of codon and amino acid use for translational functions in highly expressed cricket genes

2020 ◽  
Author(s):  
Carrie A. Whittle ◽  
Arpita Kulkarni ◽  
Nina Chung ◽  
Cassandra G. Extavour
Keyword(s):  
Amino Acids ◽  
Amino Acid ◽  
Trna Gene ◽  
Synonymous Codon ◽  
Gene Copy ◽  
Female Gonad ◽  
Optimal Codons ◽  
Gene Copies ◽  
Highly Expressed Genes ◽  
Codon Use

AbstractBackgroundFor multicellular organisms, much remains unknown about the dynamics of synonymous codon and amino acid use in highly expressed genes, including whether their use varies with expression in different tissue types and sexes. Moreover, specific codons and amino acids may have translational functions in highly transcribed genes, that largely depend on their relationships to tRNA gene copies in the genome. However, these relationships and putative functions are poorly understood, particularly in multicellular systems.ResultsHere, we rigorously studied codon and amino acid use in highly expressed genes from reproductive and nervous system tissues (male and female gonad, somatic reproductive system, brain, ventral nerve cord, and male accessory glands) in the cricket Gryllus bimaculatus. We report an optimal codon, defined as the codon preferentially used in highly expressed genes, for each of the 18 amino acids with synonymous codons in this organism. The optimal codons were largely shaped by selection, and their identities were mostly shared among tissue types and both sexes. However, the frequency of optimal codons was highest in gonadal genes. Concordant with translational selection, a majority of the optimal codons had abundant matching tRNA gene copies in the genome, but sometimes obligately required wobble tRNAs. We suggest the latter may comprise a mechanism for slowing translation of abundant transcripts, particularly for cell-cycle genes. Non-optimal codons, defined as those least commonly used in highly transcribed genes, intriguingly often had abundant tRNAs, and had elevated use in a subset of genes with specialized functions (gametic and apoptosis genes), suggesting their use promotes the upregulation of particular mRNAs. In terms of amino acids, we found evidence suggesting that amino acid frequency, tRNA gene copy number, and amino acid biosynthetic costs (size/complexity) had all interdependently evolved in this insect model, potentially for translational optimization.ConclusionsCollectively, the results strongly suggest that codon use in highly expressed genes, including optimal, wobble, and non-optimal codons, and their tRNAs abundances, as well as amino acid use, have been adapted for various functional roles in translation within this cricket. The effects of expression in different tissue types and the two sexes are discussed.

scholarly journals Adaptation of codon and amino acid use for translational functions in highly expressed cricket genes

BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Carrie A. Whittle ◽  
Arpita Kulkarni ◽  
Nina Chung ◽  
Cassandra G. Extavour
Keyword(s):  
Amino Acids ◽  
Amino Acid ◽  
Trna Gene ◽  
Synonymous Codon ◽  
Gene Copy ◽  
Female Gonad ◽  
Optimal Codons ◽  
Gene Copies ◽  
Highly Expressed Genes ◽  
Codon Use

Abstract Background For multicellular organisms, much remains unknown about the dynamics of synonymous codon and amino acid use in highly expressed genes, including whether their use varies with expression in different tissue types and sexes. Moreover, specific codons and amino acids may have translational functions in highly transcribed genes, that largely depend on their relationships to tRNA gene copies in the genome. However, these relationships and putative functions are poorly understood, particularly in multicellular systems. Results Here, we studied codon and amino acid use in highly expressed genes from reproductive and nervous system tissues (male and female gonad, somatic reproductive system, brain and ventral nerve cord, and male accessory glands) in the cricket Gryllus bimaculatus. We report an optimal codon, defined as the codon preferentially used in highly expressed genes, for each of the 18 amino acids with synonymous codons in this organism. The optimal codons were mostly shared among tissue types and both sexes. However, the frequency of optimal codons was highest in gonadal genes. Concordant with translational selection, a majority of the optimal codons had abundant matching tRNA gene copies in the genome, but sometimes obligately required wobble tRNAs. We suggest the latter may comprise a mechanism for slowing translation of abundant transcripts, particularly for cell-cycle genes. Non-optimal codons, defined as those least commonly used in highly transcribed genes, intriguingly often had abundant tRNAs, and had elevated use in a subset of genes with specialized functions (gametic and apoptosis genes), suggesting their use promotes the translational upregulation of particular mRNAs. In terms of amino acids, we found evidence suggesting that amino acid frequency, tRNA gene copy number, and amino acid biosynthetic costs (size/complexity) had all interdependently evolved in this insect model, potentially for translational optimization. Conclusions Collectively, the results suggest a model whereby codon use in highly expressed genes, including optimal, wobble, and non-optimal codons, and their tRNA abundances, as well as amino acid use, have been influenced by adaptation for various functional roles in translation within this cricket. The effects of expression in different tissue types and the two sexes are discussed.

scholarly journals Synonymous Codon Usage Analysis of Thirty Two Mycobacteriophage Genomes

2009 ◽  
Vol 2009 ◽  
pp. 1-11 ◽  
Author(s):  
Sameer Hassan ◽  
Vasantha Mahalingam ◽  
Vanaja Kumar
Keyword(s):  
Codon Usage ◽  
Synonymous Codon ◽  
Nucleotide Composition ◽  
Synonymous Codon Usage ◽  
Compositional Bias ◽  
Trna Genes ◽  
Translation Efficiency ◽  
Multivariate Statistical ◽  
Strong Negative Correlation ◽  
Highly Expressed Genes

Synonymous codon usage of protein coding genes of thirty two completely sequenced mycobacteriophage genomes was studied using multivariate statistical analysis. One of the major factors influencing codon usage is identified to be compositional bias. Codons ending with either C or G are preferred in highly expressed genes among which C ending codons are highly preferred over G ending codons. A strong negative correlation between effective number of codons (Nc) and GC3s content was also observed, showing that the codon usage was effected by gene nucleotide composition. Translational selection is also identified to play a role in shaping the codon usage operative at the level of translational accuracy. High level of heterogeneity is seen among and between the genomes. Length of genes is also identified to influence the codon usage in 11 out of 32 phage genomes. Mycobacteriophage Cooper is identified to be the highly biased genome with better translation efficiency comparing well with the host specific tRNA genes.

scholarly journals Impact of translational selection on codon usage bias in the archaeon Methanococcus maripaludis

2010 ◽  
Vol 7 (1) ◽  
pp. 131-135 ◽  
Author(s):  
Laura R. Emery ◽  
Paul M. Sharp
Keyword(s):  
Codon Usage ◽  
Codon Usage Bias ◽  
Trna Genes ◽  
Strongly Correlated ◽  
Methanococcus Maripaludis ◽  
E Coli ◽  
Moderate Growth ◽  
Optimal Codons ◽  
Genome Wide ◽  
Highly Expressed Genes

Patterns of codon usage have been extensively studied among Bacteria and Eukaryotes, but there has been little investigation of species from the third domain of life, the Archaea. Here, we examine the nature of codon usage bias in a methanogenic archaeon, Methanococcus maripaludis . Genome-wide patterns of codon usage are dominated by a strong A + T bias, presumably largely reflecting mutation patterns. Nevertheless, there is variation among genes in the use of a subset of putatively translationally optimal codons, which is strongly correlated with gene expression level. In comparison with Bacteria such as Escherichia coli , the strength of selected codon usage bias in highly expressed genes in M. maripaludis seems surprisingly high given its moderate growth rate. However, the pattern of selected codon usage differs between M. maripaludis and E. coli : in the archaeon, strongly selected codon usage bias is largely restricted to twofold degenerate amino acids (AAs). Weaker bias among the codons for fourfold degenerate AAs is consistent with the small number of tRNA genes in the M. maripaludis genome.

Analysis of codon usage patterns of the chloroplast genomes in the Poaceae family

2012 ◽  
Vol 60 (5) ◽  
pp. 461 ◽  
Author(s):  
Yuerong Zhang ◽  
Xiaojun Nie ◽  
Xiaoou Jia ◽  
Cunzhen Zhao ◽  
Siddanagouda S. Biradar ◽  
...  
Keyword(s):  
Codon Usage ◽  
Synonymous Codon ◽  
Synonymous Codon Usage ◽  
Mutational Bias ◽  
Plot Analysis ◽  
Optimal Codons ◽  
Chloroplast Genomes ◽  
Usage Patterns ◽  
Poaceae Family ◽  
High Representation

Codon usage patterns of 23 Poaceae chloroplast genomes were analysed in this study. Neutrality analysis indicated that the codon usage patterns have significant correlations with GC12 and GC3 and also showed strong bias towards a high representation of NNA and NNT codons. The Nc-plot showed that although a large proportion of points follow the parabolic line of trajectory, several genes with low ENc values lie below the expected curve, suggesting that mutational bias played a major role in the codon biology of the Poaceae chloroplast genome. Parity Rule 2 plot analysis showed that T was used more frequently than A in all the genomes. Correspondence analysis of relative synonymous codon usage indicated that the first axis explained only a partial amount of variation of codon usage. Furthermore, the gene length and expression level were also found to drive codon usage variation. These findings revealed that besides natural selection, other factors might also exert some influences in shaping the codon usage bias in Poaceae chloroplast genomes. The optimal codons of these 23 genomes were also identified in this study.

A Novel Method to Predict Highly Expressed Genes Based on Radius Clustering and Relative Synonymous Codon Usage

2015 ◽  
Vol 22 (12) ◽  
pp. 1086-1096 ◽  
Author(s):  
Tuan-Anh Tran ◽  
Nam Tri Vo ◽  
Hoang Duc Nguyen ◽  
Bao The Pham
Keyword(s):  
Codon Usage ◽  
Synonymous Codon ◽  
Synonymous Codon Usage ◽  
Relative Synonymous Codon Usage ◽  
Highly Expressed Genes ◽  
Novel Method

scholarly journals The selection-mutation-drift theory of synonymous codon usage.

Genetics ◽  
1991 ◽  
Vol 129 (3) ◽  
pp. 897-907 ◽  
Author(s):  
M Bulmer
Keyword(s):  
Codon Usage ◽  
Genetic Model ◽  
Synonymous Codon ◽  
Growth Yield ◽  
Synonymous Codon Usage ◽  
Synonymous Codons ◽  
Drift Theory ◽  
Highly Expressed Genes ◽  
Unicellular Organisms ◽  
Selection For

Abstract It is argued that the bias in synonymous codon usage observed in unicellular organisms is due to a balance between the forces of selection and mutation in a finite population, with greater bias in highly expressed genes reflecting stronger selection for efficiency of translation. A population genetic model is developed taking into account population size and selective differences between synonymous codons. A biochemical model is then developed to predict the magnitude of selective differences between synonymous codons in unicellular organisms in which growth rate (or possibly growth yield) can be equated with fitness. Selection can arise from differences in either the speed or the accuracy of translation. A model for the effect of speed of translation on fitness is considered in detail, a similar model for accuracy more briefly. The model is successful in predicting a difference in the degree of bias at the beginning than in the rest of the gene under some circumstances, as observed in Escherichia coli, but grossly overestimates the amount of bias expected. Possible reasons for this discrepancy are discussed.

scholarly journals Analysis of Codon Bias in Mitochondrial Genome of Epinephelus Fuscoguttatus

2021 ◽  
Author(s):  
Lirong Bai ◽  
Lili Lu ◽  
Suping Li ◽  
Jicui He ◽  
Jian Chen ◽  
...  
Keyword(s):  
Mitochondrial Genome ◽  
Codon Usage ◽  
Codon Bias ◽  
Synonymous Codon ◽  
Economic Value ◽  
Gc Content ◽  
Optimal Codons ◽  
Epinephelus Fuscoguttatus ◽  
The Difference ◽  
Usage Preference

Abstract Background: Epinephelus fuscoguttatus is one of the rare marine economic fishes with high economic value. At present, the researches on grouper mainly focus on artificial propagation, physiology and biochemistry, diseases and so on. However, there are few reports on mitochondrial genome level. The research aimed to analyze composition characteristics and usage preference of codon of mitochondrial genome in E. fuscoguttatus, and explored main factors of affecting the formation of codon preference, thereby providing theoretical basis for studying species evolution, genetics and breeding, and improving expression efficiency of exogenous genes. Results: GC content of mitochondrial genome of E. fuscoguttatus changed between 44.00% and 46.30%, with 45.40% of mean. Change range of CAI value was between 0.125 and 0.202, and the mean was 0.155. Effective number of codons (ENC) changed between 36.08 and 49.55, with 44.98 of mean. There were 32 codons that relative synonymous codon usage (RSCU) was more than 1, mainly ended with A/C. ENC-plot analysis found that all the genes were in the lower middle of the standard curve, and there was larger difference between actual and theoretical ENC, illustrating that codon bias was mainly affected by the choice. Correspondence analysis showed that the first axis contributed 58.85% of the difference, while the second, third and fourth axes contributed 14.59%, 7.66% and 5.43% of the difference respectively. Cumulative contribution rate of the first four vectors was 85.53%. Finally, nine optimal codons were selected: CUU, AUC, GUU, CCU, GCA, UAU, CGC, AGC and GGC.Conclusions: Codon usage preference of mitochondrial genome of E. fuscoguttatus was weak, and it preferred to use A/C terminated codon, and preference was mainly influenced by choice.

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